lnundative Release of Trichogramma for the Control of Cruciferous Lepidoptera: Preintroductory Selection of an Effective Parasitoid

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1 33 lnundative Release of Trichogramma for the Control of Cruciferous Lepidoptera: Preintroductory Selection of an Effective Parasitoid G.A. Pak Department of Entomology, Wageningen Agricultural University, P.O. Box 803 1, 6700 EH Wageningen, The Netherlands (Present address: Centre for Agriculture & Environment, P.O. Box 10015, 3505 AA Utrecht, The Netherlands) Abstract Egg parasitoids of the genus Trichogramma are the most widely used natural enemy for biological pest control in the world. Their use is restricted to lepidopterous pest species. Due to relatively cheap mass rearing systems employing factitious host species, Trichogramma are usually applied for inundative biological control: repeated releases of high numbers of parasitoids aiming at a direct control effect in the pest population. This paper discusses one of the central issues of biological control: the selection of a candidate natural enemy. Studies of the parasitization and searching behavior of Trichogramma have shown that inter- and intra-specific variability occurs for most characteristics determining their effectiveness as a control agent. A preintroduction selection procedure comparing different Trichogramma strains or species may then be useful or even necessary. This procedure requires a set of evaluation criteria and bioassays to quantify these. lnundative Biological Control Inundative biological control aims at directly increasing mortality in the pest population, whereby the released natural enemy is used as a biological insecticide (Stinner 1977). The practice of inundative release therefore centers on its cost/benefit ratio as compared to alternatives, especially pesticides. Species of the hymenopterous genus Trichogramma have been used more than any other natural enemy for inundative biological control (Ridgway and Morrison 1985). Trichogramma has a wide range of hosts, especially among the Lepidoptera (Nagarkatti and Nagaraja 1977). Suitable factitious hosts include the eggs of lepidopterous storage pests of grains, making mass production economically feasible. Experiments with Trichogramma started in the beginning of this century in the USA and the USSR. Development of a method for mass production of Trichogramma on eggs of the Angoumois grain moth Sitotroga cerealella gave rise to worldwide use of the parasitoid as a control agent. In a paper with the meaningful title Is Trichogramma becoming a fad?, Smith and Flanders (193 1) expressed their concern about the usefulness of these applications, on the grounds of a lack of convincing evidence for practical results. Because of this, and the advent of organic chemical pesticides, interest in Trichogramma faded in western countries (Ridgway et al. 1977). Research on the use of Trichogramma continued in the USSR and China, probably due to a lack of pesticides, rather than biological or economical effectiveness of Trichogramma release (Van Lenteren 1987). In these two countries application is presently carried out on several millions of hectares. Increasing problems with the use of pesticides has stimulated renewed interest in biological control, whether as a method by itself or as part of an integrated pest control system. For 297

2 298 Pak Trichogramma, this has led to commercially successful programs in Europe to control the corn borer, Ostrinia nubilalis, by inundative releases of T. maidis Pintureau and Voegelé (Hassan 1981, Bigler 1986). Prospective application of Trichogramma against numerous other lepidopterous pests throughout the world has been reviewed by Stinner (1977). Successful applications are reported for some crops, while results appear to be inconsistent for others. For example, extensive research into the control of Heliothis zea in cotton by releases of T. pretiosum Riley did not provide sufficient results to warrant general adoption of this method in the USA (King et al. 1986). Effective control of Lepidoptera on cabbage by releases of T. evanescens Westwood has been reported for the species Mamestra brassicae (Shchepetilnikova 1974, Hassan and Rost 1985), Pieris rapae (Parker et al. 1971, Parker and Pinnell 1972) and Trichoplusia ni (Zilberg 1972). Parasitism of Plutella xylostella (L.) eggs is scarcely reported in the literature. In Japan they are parasitized by T. chilonis Ishii (K. Hirai, personal communication). Egg parasitoids account for 15 % of the successful inoculative biological control agents, and their success ratio is similar to that of larval parasitoids and better than that of pupal parasitoids (Hokkanen 1985). Egg parasitoids occur in 16 families of Hymenoptera, of which the Trichogrammatidae, Mymaridae and Scelionidae are composed exclusively of egg parasitoids. Examples of successful inoculative control by egg parasitoids are known for the Scelionidae and the Mymaridae, but not for the Trichogrammatidae. Greathead (1986) therefore concluded that trichogrammatids are less successful control agents than species from the other egg-parasitoid families. Strand (1986) suggested that, for unknown reasons, Trichogramma spp. are less specialized in parasitizing certain species within their major host group (Lepidoptera) than the scelionids (specialized on Lepidoptera, Hemiptera of Orthoptera) and the mymarids (specialized on Homoptera). The preoccupation with Trichogramma, instead of other egg parasitoid, for inundative biological control seems to stem largely from its polyphagous nature and feasibility of mass production on factitious hosts, rather than from superior biological traits determining effectiveness as a control agent. Selection Of Candidate Natural Enemies The major phases in the development of a biological control program are: (1) collection of information on pest and natural enemies, (2) exploration for natural enemies, (3) selection of candidates, (4) mass production and release, and (5) evaluation of results. The selection of candidate natural enemies, which is generally considered the most critical. phase for the success of a biological control program, is an issue surrounded by conflicting ideas about the usefulness of preintroductory research. This art versus science conflict (Harris 1973) seems to be one between theoretical ecologists and practitioners of biological control. In the extreme, the theoreticians believe that it is possible to determine the best natural enemy by preintroductory studies, whereas the practitioners advocate a minimum of such studies and prefer to test each prospective candidate directly in the field by a trial-and-error method. Nevertheless, most practitioners express ideas about attributes that an effective natural enemy should possess, although they rarely seem to use these as a check list of selection criteria (Van Lenteren 1980). Selection Of Trichogramma The feasibility of mass production on factitious hosts has promoted extensive use of the egg parasitoid Trichogramma for inundative biological control programs. In production systems the hosts used are generally grain-feeding Lepidoptera such as the rice meal moth, Corcyra cephalonica, the Mediterranean flour moth, Ephestia kuehniella, and the Angoumois grain moth, Sitotroga cerealella. In addition to efficient mass production, application systems have been developed for manual delivery in small fields of 1-2 ha and aerial delivery in fields larger than 10 ha.

3 Trichogramma Selection 299 Scholz (1990) reviewed the different selection methods employed by Trichogramma workers from literature data and concluded that preintroduction evaluation studies of different candidates are carried out in less than 10% of all programs. The prospective Trichogramma strain is most often collected locally, on the grounds of expecting an optimal adaptation to pest and environment in local populations, or is imported from a colleague who uses it successfully against the same pest species (Table 1). Selecting Trichogramma by means of trial-and-error releases in the field has produced good results, but not consistently (Stinner 1977). The selection of effective parasitoid species or strains has therefore been identified as one of the necessities to improve the success record for Trichogramma application (Ridgway and Morrison 1985). Table I. Criteria used to select species of egg parasitoids for use against lepidopteran pests around the world. Method of selection Frequency (%) Pre-release evaluation Species reared from target pest Most abundant species in release region Species readily available from a research institution or biological control company Species successfully used in other countries Method of selection not specified Inter- and intra-specific variation In preintroductory selection programs of candidate natural enemies researchers make use, among others, of the fact that pest species usually have a different complex of natural enemies for different parts of their natural range. Biological differences among species or populations of natural enemies, whether morphological, physiological, ecological or behavioral, are the result of geographical variations in environmental and biological interactions and reflect adaptations in populations to the local environment. Little is known, however, about qualitative and quantitative genetic differences between conspecific populations of natural enemies which differ in biological traits. In the past, researchers have shown a certain awareness of the importance of genetic variation for the success of (inoculative) introductions of natural enemies (Remington 1968; Hoy 1985). A prolific use of different terms in the literature to characterize different populations of conspecific natural enemies, including form, race, ecotype, biotype, strain and polymorphs, bears witness of a similar awareness among practitioners of biological control (Diehl and Bush 1984). Introduction of differently adapted strains or species may improve the success of a biological control program. Messenger and Van den Bosch (1971) reviewed several examples of limited adaptiveness in geographical strains of natural enemy species, such as climatic tolerance, host specificity and evasion of host-immunity response, which reduced their effectiveness as control agents. Nevertheless, they concluded that this vast potential resource of conspecific strains of natural enemies with different ecological and behavioral adaptabilities has hardly been tapped to improve biological control. A preintroductory selection program for Trichogramma will make use of inter- and intraspecific differences between different populations of the genus. In the past, only a few species of Trichogramma were recognized, due to taxonomic difficulties (Nagarkatti and Nagaraja 1977). Differences in structure of male genitalia were used to describe new species by Nagaraja and Nagarkatti (1969) and gave rise to extensive revision of the genus (Voegelé and Pintureau 1982). Therefore, it is difficult to relate previous accounts of biological differences between ecotypes of Trichogramma (Kot 1979), or strains (Diehl and Bush 1984), with their present taxonomic status. Inter- and/ or intra-specific differences have been reported among Trichogramma for

4 300 Pak various biological characteristics (see Pak (1988) for references): (1) adaptation to plant structure or habitat, (2) adaptation to climatic conditions, (3) fecundity, (4) longevity, (5) intrinsic rate of increase, (6) host suitability, (7) walking speed, (8) parasitization rate, (9) attraction to hosts, and (10) response to searching stimulants (kairomones). Selection Criteria Consideration of current knowledge and ideas on factors determining the effectiveness of natural enemies in suppressing pest populations has led to a list of nine possible criteria for preintroductory selection of natural enemies (Van Lenteren 1986). These selection criteria are discussed below. Definitions of most of these criteria are reviewed and, as a consequence, renamed to clarify their meaning. Conclusions are summarized in Table 2, in which each criterion is given a coarse rating (low-medium-high) for three aspects; (1) usefulness to select candidate strains, (2) the amenability for manipulation by, for example, producers and users, and (3) the current level of biological understanding on the way certain traits function and may be utilized. In addition, important research areas are indicated for each criterion. Table 2. Evaluation of criteria for the selection of candidate Trichogramma strains to be used in inundative biological control programs and major research areas identified to enhance the evaluation of selection criteria. Usefulness Amenability Level of Criterion for preintroductory for manipulation knowledge or Research areas selection by applier utilization Environmental risks higha medium low Impact of releases on natural host communities Tolerance of climatic high medium medium Heritability of extreme locomotory activity Host-plant adaptation medium low low Dispersal to different habitats or plant types Host selection high low medium Host selection in natural patches; host perception Host suitabilty medium low medium Cytolytic process of killing hosts Seasonal low high high Longevity of wasps in synchronization the field Reproductive capacity medium high high Heritability of fecundity Host-finding capacity high medium low Travel speed, dispersal Culture method higha highb medium by flight, role of kairomones In vitro culture, quality of produced wasps ªConditional necessity rather than selection criterion for research program. 'Manipulation by producer Environmental risks Serious negative aspects of natural enemies, such as (facultative) hyperparasitic habits of parasitic wasps or predation upon other beneficial species, may impede their use for any method of biological control. However, the primary concern is not with the negative trait itself, but rather with the degree of risk it may pose to the environment. Environmental risk therefore seems to be a more suitable term for this criterion. Inundative biological control involves repeated releases of large numbers of natural enemies into crops. The possible impact of releases on alternative hosts in surrounding (natural) habitats

5 Trichogramma Selection 30 1 should therefore be investigated as part of the development of the control program. Registration of biological control agents, comparable to that of pesticides, will probably become a regulation, which will require criteria to test their environmental safety. Trichogramma inundations are considered safe by appliers, perhaps because they usually release local strains collected from the pest species. However, if an exotic strain is released, or one that has been artificially selected, the possibility of increased egg parasitism of Lepidoptera other than the pest species itself is not imaginary, especially since most Trichogramma species are polyphagous. Permanent establishment of exotic species might be avoided by selecting strains which, for example, cannot overwinter in the new environment. Tolerance of climatic extremes Climatic adaptation involves the ability of natural enemies to effectively control a pest under ambient climatic conditions. However, in a broader sense, climatic adaptation concerns the ability of natural enemies to tolerate the extreme abiotic conditions of their environment. Climatic tolerance is a determining factor for the survival and/or the reproduction of a natural enemy. For inoculative introductions, survival under extreme conditions is an essential prerequisite for colonization, even if reproduction is limited to periods of more favorable conditions. For seasonal inoculative and inundative introductions the ability to reproduce is of immediate importance and should not be restricted by abiotic conditions. In Trichogramma, tolerance to extreme environmental conditions has been primarily studied for high temperatures. However, in countries with a temperate climate, low temperatures may be a major limiting factor to the parasitization activity of Trichogramma females (see host-finding capacity). Significant variations in proportional activity (i.e. the number of females engaged in locomotory and parasitization activity) at 12 C were found by Pak and Van Heiningen (1985) between geographical strains and appeared to correspond to the performance of strains of different activity released in the field (Pak et al. 1989). Temperature dependence of parasitoid activity, therefore, appears to be a useful criterion to select candidate strains for evaluation programs. Host-plant adaptation The ability to attack a given species of host on all economically important host plants is considered important for inoculative biological control, but not for seasonal inoculative and inundative biological control. For the latter methods it has been suggested that a variable effectiveness of a natural enemy for different host plants of its (polyphagous) insect host is amenable for manipulative correction, e.g. by releasing more enemies. Different rates of egg parasitism are reported for the same host species on different plant types, usually by different Trichogramma spp. (Martin et al. 1981; Lopez et al. 1982). Hostplant adaptation may be involved in host-habitat location, which has been demonstrated by Altieri et al. (1981) and Nordlund et al. (1985). Furthermore, Trichogramma species appear to be adapted to different plant structures (Thorpe 1985). Host-plant adaptations probably interact with hostspecies adaptations, and their combined effect results in strains of Trichogramma being specialized and released in different crops, for example T. maidis against the corn borer, O. nubilalis, and T. pretiosum against the cotton bollworm, H. zea. Host specificity Host specificity concerns the range of different host ages and host species accepted by the parasitoid. As a selection criterion host specificity is related to other criteria, such as environmental risks (narrow host range and low propensity of hyperparasitism), host suitability and density responsiveness (high host-finding capacity). If the latter criteria are evaluated for candidate parasitoids, host specificity might be investigated separately. Alternatively, a study of host specificity might be sufficient to permit evaluation of the other criteria also.

6 302 Pak For inundative and seasonal inoculative releases host specificity is not considered an important selection criterion, apparently due to the assumption that releases are directed against a single pest species (Van Lenteren 1980). However, if two or more related species are to be controlled, the use of a single effective parasitoid is probably more economical (in costs of development of the program) than the use of different parasitoids for each host species. Host specificity, therefore, should be considered as an important selection criterion, because the occurrence of related host species in the same crop is not exceptional (Ehler and Miller 1978). Pak et al. (1986) and Pak et al. (1990b) studied variability among Trichogramma strains for host-age and host-species selection of host species occurring on cabbage crops. The preferred ages of different species of host eggs had to be determined before host-species selection experiments could be carried out. The effectiveness of a parasitoid may be reduced if host acceptance is limited to certain ages of hosts. Host age selection scarcely occurred, but females of 9 out of 12 strains tested for host species selection preferred Mamestra brassicae eggs over Pieris brassicae and P. rapae eggs as a host. Host-species selection turned out te be a useful criterion for the selection of candidate strains, because parasitism of Pieris eggs in the field was predominantly observed for a strain that did not show a preference for either of the host species in the laboratory (Pak et al. 1989). Host suitability Host suitability concerns the ability of the parasitoid to complete development in the host and seems a more direct term for this criterion than internal synchronization. It was not considered an important selection criterion for inundative releases by Van Lenteren (1980), because their aim may be fulfilled if the host is killed. However, if host eggs are not always killed when attacked (Pak et al. 1990a), host suitability should be considered as a criterion in the selection of candidate strains. Seasonal synchronization Seasonal synchronization with the host refers to the temporal (external) correspondence between the proper stages of the life cycles of host and parasitoid. For inundative biological control, natural synchronization is not an important criterion. The applier can synchronize populations of the parasitoid and the host by introducing the parasitoids at the proper time. In fact, inundative releases are a way of artificially synchronizing the occurrence of hosts and sufficient numbers of parasitoids in places where they are actually poorly synchronized. Host phenology, especially host-egg density, determines decisions regarding the timing and frequency of releases. Thus, the presence of host eggs must be regularly monitored or predicted by means of model computations (Ridgway et al. 1981). The age of host eggs may significantly affect their susceptibility to parasitism by Trichogramma (Pak 1986). Since young eggs are generally most susceptible, it may be of crucial importance that female wasps are searching for host eggs from the beginning of the oviposition period of the host insect. Trichogramma are usually introduced into the field as immatures in the pupal or pharate adult stage, mechanically or by hand. In the laboratory, wasps fed with honey may live for a few weeks at moderate temperatures, but little is known about the life span of females in the field. Under variable, unpredictable weather conditions the introduction of parasitoid pupae of mixed ages into the field may provide for a continuous supply of sufficient foraging wasps for several weeks (Hassan 1982; Bigler 1986). Reproductive capacity The potential reproductive capacity of a natural enemy is usually expressed by the intrinsic rate of natural increase value) which combines development time and mortality of immatures, adult survival and fecundity into the rate of population growth (Pak and Oatman

7 Trichogramma Selection b). Parasitoids develop to the detriment of their hosts (solitary or gregariously), and may also kill them by host feeding. Thus, the host-death rate caused by activity of the parasitoids should offset the rate of increase of the host in the absence of parasitoids (Van Lenteren 1986). The potential reproductive impact on the host population is usually determined in the laboratory under optimal conditions of host availability. In practice, however, parasitoids may not find the hosts as readily as in the laboratory and, consequently, the field host-death rate per female parasitoid may be lower. For inundative biological control the reproductive potential does not appear to be a useful selection criterion, because a limited parasitoid fecundity can, in theory, be adjusted by releasing more parasitoids. However, Smith and Hubbes (1986) did find that differences in field performance between various indigenous geographical strains of T. minutum, in parasitism of spruce budworm eggs, Choristoneura fumiferana, corresponded to differences in reproductive capacity between strains determined in the laboratory. If host eggs are laid in clusters rather than singly, the effectiveness of a parasitoid as a control agent may be reduced if a single female cannot parasitize all hosts in a patch. Field observations by Pak et al. (1989) showed that the fecundity of Trichogramma females may be too low to parasitize each egg in clusters of M. brasssicae containing more than 20 eggs, which make up a considerable fraction of the egg population, especially toward the end of the season. Thus if the biological control effectiveness of wasps is limited by their reproductive capacity, fecundity might be a useful selection criterion for inundative biological control. Host-finding capacity Density responsiveness is often mentioned as a selection criterion related to the host-finding ability of natural enemies. The question of density-dependent host-parasitoid interactions, such as spatial heterogeneity, parasitoid aggregation and mutual interference, is of great interest in the theory of population regulation by effective natural enemies (Waage and Hassell 1982). As a result, density-dependent behavior is commonly seen as an essential feature of the searching efficiency or capacity of candidate natural enemies, but it also seems to be the most difficult selection criterion for experimental evaluation (Van Lenteren 1986). Coexistence of pest and natural enemy at a low density seems to be an essential feature of inoculative and seasonal inoculative biological control, but not of inundative biological control. In addition to density-dependent behavioral responses of parasitoids, any trait of their searching behavior that has a significant influence on the probability of host-finding might be a useful selection criterion, especially traits related to the searching effort (travel speed, travel time and responses to searching stimulants). Since the measure of success of a natural enemy is in the actual finding of hosts rather than in the searching for hosts, host-finding capacity seems the most appropriate term for this criterion. The host-finding capacity of a parasitoid is the number of hosts found per unit of time. However, this does not seem to be a useful measure for evaluation, because it is only conveniently determined under controlled conditions at a relatively high host density (Hassell, 1986). At a high host density, the host-finding capacity of a parasitoid is limited by her egg complement and/or by her handling time. However, in fields with relatively low host densities, and especially when host eggs are laid in clusters, wasps may be foraging a lot on leaves without hosts (Pak et al. 1989). The host-parasitoid interaction occurring in the field suggests that it is practically unrealistic to express the host-finding capacity of inundatively released Trichogramma in terms of an absolute deterministic measure, such as the area traversed or the area of discovery. These measures assume that parasitoids search randomly, whereas it is becoming increasingly apparent that host searching is directed or stimulated by physical or chemical cues from the habitat or host, substances functioning as synomones of kairomones. Analysis of host-finding differences among Trichogramma in the laboratory seems' to be feasible. For example, Bigler et al. (1988) found that differences in travel speed between a number

8 304 Pak of strains of T. maidis in the laboratory corresponded consistently, i.e. for several seasons, to differences in performance in the field. This suggests that travel speed might be a useful measure to select strains. Another possibility to select Trichogramma strains might be based on differences in the response of females to kairomones. Contact kairomones are present in the wing scales of adult hosts and are deposited by ovipositing females on and around the eggs (Gross 1981). In addition, the sex pheromone of the adult-female host has been found to function as volatile kairomone for Trichogramma, probably playing a role in host community location (Lewis et al. 1982). Since sex pheromone is a more host-specific kairomone source than host scales (Noldus 1989), inter- and intra-specific differences in kairomonal responses among Trichogramma strains may be more common for volatile than for contact kairomones. Culture method A good culture method is an essential prerequisite for the use of a natural enemy in seasonal inoculative and inundative biological control programs. The ability to culture a given natural enemy is a conditional necessity of concern to the producer, rather than a useful selection criterion for the researcher conducting an evaluation program. The widespread use of Trichogramma as an inundatively released control agent is a consequence of the feasibility of mass production on factitious host species. However, host-specific species or strains, such as T. nubilale, cannot be readily cultured on factitious host eggs, which may limit their practical use (Burbutis and Goldstein 1983). Host species commonly used to mass-produce Trichogramma have relatively small eggs, which produce small Trichogramma. Smaller Trichogramma females generally have a lower fecundity, a shorter longevity and a lower walking speed than larger females from natural hosts. In the past, the quality of mass-produced Trichogramma has received little attention from practitioners, although several accounts of reduced field effectiveness have been reported for laboratory cultures of strains. Adverse genetic changes that might take place in mass-cultured strains should be monitored in order to maintain the quality of Trichogramma as a control agent. Population-genetic studies and the monitoring of the quality of mass-produced parasitoids require the quantification of biological traits (Bigler et al. 1987), for which several of the presently discussed selection criteria may be useful. Improving Trichogramma effectiveness If an effective wild strain of Trichogramma cannot be found in nature, it might be possible to improve the effectiveness of existing laboratory strains. The major approaches suggested toward this aim are enhancement of the activity of releases of parasitoids in the field, and genetic improvement of a strain by selective breeding. Trichogramma has been the subject of extensive research on manipulation of the searching behavior by the application of contact or volatile kairomonal substances to the habitat, which primarily at low host densities might increase the effectiveness of host finding (Gross 1981). Gross et al. (1981) demonstrated that prerelease oviposition and kairomone experience may stimulate searching behavior and increase retention time of wasps in a target area. This response might suppress dispersal of the wasps from a crop habitat. In order to reinforce the response to contact kairomones applied to the habitat, Gross et al. (1984) distributed supplemental (sterilized) host eggs in the field, which increased the rate of finding natural hosts. The present research on selection criteria to evaluate the effectiveness of Trichogramma strains may be useful in directing which qualitative traits need genetic improvement of the parasitoids, because the lack of criteria to measure quality or to direct linear selections appears to be a major limiting factor for putting ideas into practice (Hoy 1976). If natural selection acts against the artificially selected trait, or if outbreeding with a natural population occurs, an artificially selected enemy will gradually revert to a wild genotype after inoculative introduction. The prospects of genetic improvement seem to be especially promising for inundatively introduced

9 Trichogramma Selection 305 natural enemies, because this method offers the opportunity to maintain the quality of the selected trait of a strain by applying a continuous selection pressure in the mass production. Art Or Science Inundative biological control is a technical enterprise, which offers opportunities to leave behind the primitive hunting-and-gathering phase of biological control (Hoy 1979). The trialand-error approach to the selection of candidate control agents has been a useful element of this phase. In the past, several ecologists and entomologists have expressed their concerns about the orthodox approach to the choice of effective natural enemies. Krebs (1972) commented that until we can explain why an introduction program is a success or a failure, biological insect pest suppression will remain an art, not a science. Van Lenteren (1980) discussed the question of whether the art does have to become a science, while Hokkanen (1985) suggested that the selection of effective natural enemies should probably best be regarded as an art, based on science. I believe that if biological control is to gain wide adoption as a method of pest control, it needs to be based on research by scientists, who should enjoy art to give relaxation to their puzzled and weary minds. These scientists should study behavioral interactions between natural enemies and their hosts or prey in order to find useful criteria and methods to evaluate or monitor the effectiveness of candidate natural enemies. References Altieri, M. A., Lewis, W. J., Nordlund, D. A., Gueldner, R. C., and Todd, J. W Chemical interations between plants and Trichogramma wasps in Georgia soybean fields. Prot. Ecol., 3, Bigler, F., Mass-production of Trichogramma maidis Pint. et Voeg. and its field application against Ostrinia nubinalis Hbn. in Switzerland. J. Appl. Entomol., 101, Bigler, F., Meyer, A., and Bosshart, S Quality assessment in Trichogramma maidis Pintureau et Voegele reared from eggs of the factitious hosts Ephestia kuehniella Zell. and Sitotroga cerealella (Olivier). J. Appl. Entomol., 104, Bigler, F., Bieri, M., Fritschy, R., and Seidel, K Locomotive activity of Trichogramma maidis Pint. et Voeg. and its relation to parasitism of eggs of Ostrinia nubilalis Hbn. Entomol. Exp. Appl., 49, Burbutis, P. P., and Goldstein, L. F Mass rearing Trichogramma nubilale on European corn borer, its natural host. Prot. Ecol., 5, Diehl, S. R., and Bush, G. L An evolutionary and applied perspective of insect biotypes. Ann. Rev. Entomol., 29, Ehler, L. E., and Miller, J. C Biological control in temporary agroecosystems. Entomophaga, 23, Greathead, D. J Parasitoids in classical biological control. In: Waage, J. K., and Greathead, D. J. (ed.). Insect parasitoids. Acad. Press, London, Gross, H. R. Jr Employment of kairomones in the management of parasitoids. In: Nordlund, D. A., Jones, R. L., and Lewis, W. J. (ed.) Semiochemicals, their role in pest control. Wiley, New York, Gross, H. R. Jr., Lewis, W. J., and Nordlund, D. A Trichogramma pretiosum: Effect of prerelease parasitization experience on retention in release areas and efficiency. Environ. Entomol., 10, Gross, H. R., Jr., Lewis, W. J., Beevers, M., and Norlund, D. A Trichogramma pretiosum (Hymenoptera: Trichogrammatidae): Effects of augmented densities and

10 distributions of Heliothis zea (Lepidoptera: Noctuidae) host eggs and kairomones on field performance. Environ. Entomol., 13, Harris, P The selection of effective agents for the biological control of weeds. Can. Entomol., 105, Hassan, S. A Mass-production and utilization of Trichogramma. 2. Four years successful biological control of the European corn borer. Med. Fac. Landbouww, Rijksuniv. Gent. 46, Mass-production and utilization of Trichogramma. 3. Results of some research projects related to the practical use in the Federal Republic of Germany. In: Les Trichogrammes, ler Symposium International, Antibes, France. Les colloques de l INRA 9, Hassan, S. A., and Rost, W. M Mass-production and utilization of Trichogramma: 6. Studies towards the use against cabbage lepidopterous pests. Med. Fac. Landbouww. Rijksuniv. Gent, 50, Hassell, M.P Parasitoids and population regulation. In: Waage, J.K., and Greathead, G.J. (ed.) Insect parasitoids. London: Academic Press, Hokkanen, H. M. T., Success in classical biological control. C RC Critical Rev. Plant Sci., 3, Hoy, M. A Genetic improvement of insects: fact or fantasy? Environ. Entomol., 5, The potential for genetic improvement of predators for pest management programs. In: Hoy, M. A., and McKelvey J. J. (ed.) Genetics in relation to insect management. Rockefeller Foundation, Improving establishment of arthropod natural enemies. In: Hoy, M. A., and Herzog, D. C. (ed.) Biological control in agricultural IPM systems. Acad. Press, Orlando, King, E. G., Bouse, L. F., Bull, D. L., Coleman, R. L., Dickerson, W. A., Lewis, W. J., Lopez, J. D., Morrison, R. K., and Phillips, J. R Management of Heliothis spp. in cotton by augmentative releases of Trichogramma pretiosum. J. Appl. Entomol., 101, Kot, J Analysis of factors affecting the phytophage reduction by Trichogramma Westw. species. Pol. Ecol. Stud., 5, Krebs, J. C. J The experimental analysis of distribution and abundance. Harper & Row, New York. Van Lenteren, J. C Evaluation of control capabilities of natural enemies: Does art have to become science? Neth. J. Zool., 30, Evaluation, mass production, quality control and release of entomophagous insects. In: Franz, J. J. (ed.) Biological plant and health protection. Fisher Verlag, Stuttgart, Environmental manipulation advantageous to natural enemies of pests. In: Delucchi, V. (ed.) Integrated pest management. Quovadis? Parasitis, Geneva, Lewis, W. J., Nordlund, D. A., Gueldner, R. C., Teal, P. E. A. and Tumlinson, J. H Kairomones and their use for management of entomophagous insects. XIII. Kairomonal activity for Trichogramma spp. of abdominal tips, excretion, and a synthetic sex pheromone blend of Heliothis zea moths. J. Chem. Ecol., 8, Lopez, J. D. Jr., Jones, R. L., and House, V. S Species of Trichogramma parasitizing eggs of Heliothis spp. and some associated lepidopterous pests in Central Texas. South w. Entomol., 7, Martin, P. B., Lindgren, P. D., Greene, G. L., and Grissell, E. E The parasitoid complex of three noctuids (Lep.) in a northern Florida cropping system: seasonal occurrence, parasitization, alternate hosts and influence of host habitat. Entomophaga, 26, Messenger, P. S., and Van den Bosch, R The adaptability of introduced biological control agents. In: Huffaker, C. B. (ed.) Biological control. Plenum. New York, Nagaraja, H., and Nagarkatti, S Three new species of Trichogramma (Hymenoptera, Trichogrammatidae) from India. Entomophaga, 14,

11 Trichogramma Selection 307 Nagarkatti, S., and Nagaraja, H Biosystematics of Trichogramma and Trichogrammatidae species. Ann. Rev. Entomol., 22, Noldus, L. P. J. J Semiochemicals, foraging behaviour and quality of entomophagous insects for biological control. J. Appl. Entomol., 108, Nordlund, D. A., Chalfant, R. B., and Lewis, W. J Response of Trichogramma pretiosum females to extracts of two plants attacked by Heliothis zea. Agric. Ecosyst. Environm., 12, Pak, G. A Behavioural variations among strains of Trichogramma spp: A review of the literature on host-age selection. J. Appl. Entomol Selection of Trichogramma for inundative biological control. A study of behavioural variations among strains and species of an egg-parasite genus. Doctorate dissertation, Wageningen Agricultural University, The Netherlands, 224 p. Pak, G. A., Buis, H. C. E. M., Heck, I.C.C., and Hermans, M. L. G Behavioural variations among strains of Trichogramma spp: Host-age selection. Entomol. Exp. Appl., 40, Pak, G. A., Van Dalen, A., Kaashoek, N. K., and Dijkman, H. 1990a. Host egg chorion structure influencing host suitability for the egg parasitoid Trichogramma Westwood. J. Insect Phys., 36, Pak, G. A., and Van Heiningen, T. G Behavioural variations among strains of Trichogramma spp: Adaptability to field-temperature conditions. Entomol. Exp. Appl., 38, Pak, G. A,, Van Heiningen, T. G., Van Alebeek, F. A. N., Hassan, S. A., and Van Lenteren, J. C Experimental inundative releases of different strains of the egg parasite Trichogramma in Brussels sprouts. Nath. J. Plant Path., 95, Pak, G. A., Kaskens, J. W. M., and De Jong E. J. 1990b. Behavioural variations among strains of Trichogramma spp.: Host-species selection. Entomol. Exp. Appl., 56, Pak, G. A., and Oatman, E. R. 1982a. Biology of Trichogramma brevicapillum. Entomol. Exp. Appl., 32, b. Comparative life table, behavior and competition studies of Trichogramma brevicapillum and T. pretiosum. Entomol. Exp. Appl., 32, Parker, F. D., Lawson, F. R., and Pinnell, R. E Suppression of Pieris rapae utilizing a new control system: Mass releases of both the pest and its parasites. J. Econ. Entomol., 64, Parker, F. D., and Pinnell, R. E Further studies of the biological control of Pieris rapae using supplemental host and parasite releases. Environ. Entomol., 1, Remington, C. L The population genetics of insect introduction. Ann. Rev. Entomol., 13, Ridgway, R. L., King, E. G., and Carrillo, J. L Augmentation of natural enemies for control of plant pests in the Western Hemisphere. In: Ridgway, R. L., and Vinson, S. E. (ed.). Biological control by augmentation of natural enemies. Plenum, New York, Ridgway, R. L., Ables, J. R., Goodpasture, C., and Hartsack, A. W Trichogramma and its utilization for crop protection in the USA. In: Proc. joint American-Soviet conference on use of beneficial organisms in the control of crop pests. Washington D.C., Entomol. Soc. Am. Bull., 1387, Ridgway, R. L., and Morrison, R. K Worldwide perspective on practical utilization of Trichogramma with special reference to control of Heliothis on cotton. Southw. Entomol. Suppl., 8, Scholz, B.C.G Pre-release evaluation studies of egg parasitoids for the management of Heliothis in Australian cotton. Master of Science Thesis. University of Queensland. St Lucia, Australia. Shchepetilnikova, V. A Use of Trichogramma in the U.S.R.R. In: Shumakov, E. M., Gusev, G. V., and Fedorinchik, N. S. (ed.). Biological agents for plant protection. Kolos, MOSCOW,

12 308 Pak Smith, H. S., and Flanders, S. E Is Trichogramma becoming a fad? Econ. Entomol. 24, Smith, S. M., and Hubbes, M Strains of the egg parasitoid Trichogramma minutum Riley. II. Utilization for release against the spruce budworm. J. Appl. Entomol., 102, Stinner, R. E Efficacy of inundative releases. Ann. Rev. Entomol., 22, Strand, M. R The physiological interactions of parasitoids with their hosts and their influence on reproductive strategies. In: Waage J. K., and Greathead, D. J. (ed.) Insect Parasitoids. Acad. Press, London, Thorpe, K. W Effects of height and habitat type on egg parasitism by Trichogramma minutum and T. pretiosum (Hymenoptera: Trichogrammatidae). Agric. Ecosyst. Environm., 12, Voegele, J., and Pintureau, B Caracterisation morphologique des groupes et especes du genre Trichogramma Westwood. In: Les Trichogrammes, ler symposium international, Antibes, France. Les Colloques de l LNRA, 9, Waage, J. K., and Hassell, M. P Parasitoids as biological control agents a fundamental approach. Parasitology, 84, Zilberg, L. P Efficiency of Trichogramma in northern zone of Moldavia. J. Biol. Plant Prot. Probl. Kishinev, 1,